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Hemiptera: Cicadellidae) in Serbia BioInvasions Records (2021) Volume 10, Issue 3: 544–554 CORRECTED PROOF Rapid Communication The “code red” for Balkan vineyards: occurrence of Orientus ishidae (Matsumura, 1902) (Hemiptera: Cicadellidae) in Serbia Tatjana Cvrković1,*, Jelena Jović1, Miljana Jakovljević1, Oliver Krstić1, Slavica Marinković1, Milana Mitrović1 and Ivo Toševski1,2 1Department of Plant Pests, Institute for Plant Protection and Environment, Banatska 33, 11080 Zemun, Serbia 2CABI, 1 Rue des Grillons, 2800 Delémont, Switzerland Author e-mails: [email protected] (TC), [email protected] (JJ), [email protected] (MJ), [email protected] (OK), [email protected] (SM), [email protected] (MM), [email protected] (IT) *Corresponding author Citation: Cvrković T, Jović J, Jakovljević M, Krstić O, Marinković S, Mitrović M, Abstract Toševski I (2021) The “code red” for Balkan vineyards: occurrence of Orientus Orientus ishidae (Matsumura, 1902) (Hemiptera: Cicadellidae), known as the ishidae (Matsumura, 1902) (Hemiptera: mosaic leafhopper, is an invasive alien species native to the Eastern Palaearctic, but Cicadellidae) in Serbia. BioInvasions also widespread and well established on the eastern territory of North America. Records 10(3): 544–554, https://doi.org/10. Since its first detection in Europe in 1998, this polyphagous species has expanded 3391/bir.2021.10.3.04 its distribution area and rapidly spread through central and western European countries, Received: 14 September 2020 inhabiting a wide range of broadleaf trees and shrubs (e.g. Gleditsia triacanthos, Accepted: 8 February 2021 Salix spp., Corylus spp., Acer spp., Betula spp., Populus spp. and Carpinus spp.), Published: 31 March 2021 which are usually present in the surrounding of vineyards. Over the last decade, Handling editor: Wolfgang Rabitch O. ishidae was frequently found within European vineyards and was proven to be Thematic editor: Angeliki F. Martinou able to complete its life cycle on grapevine. Moreover, this leafhopper was shown to be naturally infected with the Flavescence dorée phytoplasma (FDp), a devastating Copyright: © Cvrković et al. disease which causes significant economic losses in the major vine-producing This is an open access article distributed under terms of the Creative Commons Attribution License countries. This study provides data on the occurrence of O. ishidae in Serbia, clearly (Attribution 4.0 International - CC BY 4.0). confirming that it has expanded its distribution range to the Balkan Peninsula which OPEN ACCESS. could lead to establishment of new FDp epidemiological cycles inside the local vineyard regions. As a consequence, there could be an increased negative impact on phytosanitary situation with a continual spread of this vector species and FDp epidemic outbreaks in Southeastern Europe. Key words: the mosaic leafhopper, invasive alien species, Flavescence dorée phytoplasma, insect vector Introduction The mosaic leafhopper Orientus ishidae (Matsumura) (Hemiptera, Cicadellidae) is an invasive alien species which originates from the Eastern Palaearctic with a wide range of distribution, reported from Japan, Korea, Taiwan and the Philippines (EPPO 2015). Outside of its native range, O. ishidae was recorded for the first time on the territory of the USA in the early nineteenth century, where it was introduced probably via import of ornamental plants of Aralia spinosa (Sanders and DeLong 1919). It is a polyphagous species, inhabiting a wide range of broadleaf trees such as Cvrković et al. (2021), BioInvasions Records 10(3): 544–554, https://doi.org/10.3391/bir.2021.10.3.04 544 Occurrence of Orientus ishidae in Serbia Figure 1. Current distribution of Orientus ishidae (Matsumura, 1902) in Europe. First records are indicated with year denoted in the circles. Map from d-maps.com (https://d-maps.com/carte.php?num_car=2232&lang=en). Gleditsia triacanthos, Salix spp., Corylus spp., Acer spp., Betula spp., Populus spp. and Carpinus spp. (Valley and Wheeler 1985; Nickel 2010). The first record from Europe dates back to 1998 from northern Italy (Guglielmino 2005). Since its first detection, O. ishidae has expanded its range and rapidly spread through central and western European countries: Switzerland (Günthart and Mühlethaler 2002), Germany (Nickel and Remane 2003), Slovenia (Seljak 2004), Austria (Holzinger 2009), Czech Republic (Malenovský and Lauterer 2010), France (Mifsud et al. 2010), Hungary (Koczor et al. 2013), the Netherlands (den Bieman and van Klink 2015), Great Britain (EPPO 2015), Poland (Klejdysz et al. 2017), Romania (Chireceanu et al. 2017) and Belgium (Lock 2019) (Figure 1). Due to its association with wild plants in vineyard surroundings in the areas severely affected by devastating diseases of grapevine yellows phytoplasmas, the mosaic leafhopper has gained special attention over the last decade and has become a research focus in viticultural regions across Europe (Mehle et al. 2010; Lessio et al. 2016, 2019; Casati et al. 2017). Placing focus on O. ishidae is justifiable, considering that alien invasive hemipteran species play an important role as phytoplasma vectors in new environments (D’Urso et al. 2019) and can even cause epidemic outbreaks (reviewed in Constable 2010). The best example of this is the epiphytotic outbreak of the Flavescence dorée (FD) in European vineyards (reviewed in Jeger et al. 2016). Cvrković et al. (2021), BioInvasions Records 10(3): 544–554, https://doi.org/10.3391/bir.2021.10.3.04 545 Occurrence of Orientus ishidae in Serbia The Flavescence dorée phytoplasma (FDp, taxonomic subgroups 16SrV-C and 16SrV-D) is a phloem-limited plant pathogenic bacteria, which causes the most serious phytoplasma quarantine disease of grapevine in European Union (EU) and EPPO region, with severe economic consequences in the major vine-producing countries (Jeger et al. 2016). The principal insect vector of FDp in European vineyards is a leafhopper of North American origin, Scaphoideus titanus (Hemiptera: Cicadellidae), which feeds primarily on grapevine, spreading the disease from plant to plant in an epidemic manner (reviewed in Constable 2010). However, the finding of several wild plant taxa carrying FDp-related genotypes (Alnus glutinosa, A. incana, Clematis vitalba, Ailanthus altissima, Salix spp. and Corylus avellana) indicate an open transmission cycle of the disease (Angelini et al. 2004; Arnaud et al. 2007; Filippin et al. 2009, 2011; Casati et al. 2017; Malembic-Maher et al. 2020). In addition, several studies have revealed that other polyphagous planthoppers and/or leafhoppers are involved in the dispersal of FDp from wild reservoir plants into vineyards. The native planthopper, Dictyophara europaea, is able to transmit FDp from infectious C. vitalba to the grapevine (Filippin et al. 2009; Krstić et al. 2018), while native leafhoppers Oncopsis alni, Allygus modestus and A. mixtus could transmit FDp sourced from Alnus spp. (Maixner et al. 2000; Malembic-Maher et al. 2020). Recently, alien O. ishidae has been identified as an additional serious risk for spreading epidemic genotypes of FDp in Slovenia, Italy, Switzerland and France (Mehle et al. 2010; Gaffuri et al. 2011; Trivellone et al. 2015; Malembic-Maher et al. 2020). Over the last decade, O. ishidae has been frequently found in European vineyards and their vicinity and was proven to complete its life cycle on the grapevine (Lessio et al. 2019). Moreover, it was shown to be naturally infected with FDp (Mehle et al. 2010) and to be able to transmit this phytoplasma to the grapevine after experimentally forced acquisition (Lessio et al. 2016) and among naturally infected European alders (Malembic-Maher et al. 2020). In Serbian vineyards, the FDp epidemic outbreaks and occurrence of S. titanus were recorded for the first time in 2003 (Duduk et al. 2004; Magud and Toševski 2004). The role of D. europaea as a native vector and C. vitalba as an FDp reservoir plant were subsequently evidenced (Filippin et al. 2009), along with Alnus spp. as natural carriers of FDp-related genotypes (Cvrković et al. 2008). Despite all efforts to control the pathogen, FDp nowadays still spreads in Serbian vineyards and affects all grape-growing regions. For this reason and because of the documented importance of O. ishidae as an alternative vector in transmission routes of FDp, the occurrence of this leafhopper has been intensively monitored over the past decade across Serbia. This study clearly shows that O. ishidae has expanded its range to the Balkan Peninsula, indicating a potential negative impact on the phytosanitary situation as a consequence of further spread of this leafhopper and of FDp outbreaks in southeastern Europe. Cvrković et al. (2021), BioInvasions Records 10(3): 544–554, https://doi.org/10.3391/bir.2021.10.3.04 546 Occurrence of Orientus ishidae in Serbia Materials and methods During a study of Auchenorhyncha fauna in the wine-growing regions of Serbia, including Central Serbia (Belgrade, Topola), South-East Serbia (Niš, Pirot) and the Provence of Vojvodina in North Serbia (Subotica, Fruška Gora, Vršac), extensive monitoring was undertaken in diverse natural ecosystems, in deciduous trees along river banks, in forest margins and ornamental trees in urban areas where trees and shrubs reported as preferred hosts for O. ishidae were present. The surveys were made every 15 days from July to September between 2013 and 2020. The insects were collected for 15 minutes at each location, with standard entomological sweep nets and mouth aspirators. Number of adults
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